Download THE ROLES OF VARIOUS FUNCTIONAL GROUPS OF

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4. DECOMPOSITION: THE ROLES OF VARIOUS FUNCTIONAL GROUPS OF
ORGANISMS
L.Brussaard
DLO-Institute forSoil FertilityResearch,
P.O.Box30003
9750RAHaren
The Netherlands
and
Agricultural University
Department of Soil Science andGeology
P.O. Box37
6700AA Wageningen
The Netherlands
Decomposition of organic matter is largely a biological process, regulated by
decomposer organisms, the physicochemical environment and the resource quality.
The process is inseparably linked with the synthesis of new organic compounds
(biosynthesis of decomposer tissues and humification) and the release of elements
(mineralization) (Swift et al., 1979).The organisms involved in decomposition cover a
wide range of sizes: micro-organisms (bacteria, fungi), microfauna (protozoa,
nematodes), mesofauna (e.g. enchytraeids, mites, collembola, termites) and
macrofauna (e.g. earthworms). Most of the process takes place below-ground and at
the soil surface. Decomposition can be studied in terms of the contribution of the
organisms involved at the level of the individual, the population and/or the
community. Because it is impossible to study every species in soil (since there are so
many) species are often assembled in functional groups, i.e. groups that are
considered to have approximately the same function in soil. In theory such species
may belong to different taxonomical orders. Functional groups, however, are defined
such that they must be roughly homogeneous in habitat, food, feeding mode and
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ecophysiology of the organisms (Hunt et al, 1987; Moore et al., 1988). As a
consequence the boundaries usually occur between orders or lower taxa. The
subdivision in functional groups is very much determined by our taxonomie and
ecological knowledge of those groups, which in turn is largely determined by the
techniques to isolate and quantify organisms from soil. Protozoa, e.g., can be isolated
from soil but are very difficult to quantify, (Stout et al., 1982)while it is assumed that
most of the bacteria and fungi from soil are not isolated by current techniques at all
(Paul and Clark, 1989). This is one reason why decomposition is often studied in
terms of sum parameters (microbial biomass, soil respiration, enzyme activity, net
element mineralization).
Whereas sum parameters may allow a reliable description of decomposition, they are
less useful for explaining and predicting the process. Various efforts to that end have
been made starting from the food web concept. Many food web studies of natural and
agro-ecosystems (figure 1) resulted in the same figure of approximately 30% for the
contribution of the soil fauna to the transfer of nitrogen in soil, with protozoa being
the most important animal group, followed by nematodes (Verhoef and Brussaard,
1990). The contribution to carbon transfer is mostly relatively high as compared to
nitrogen transfer if the C:N ratio of the food is higher than that of the consumer.
Depending on conversion efficiencies nitrogen is usually immobilized. The
contribution to carbon transfer is mostly relatively low as compared to nitrogen
transfer if the C:N ratio of the food is approximately the same as that of the
consumer or smaller. Again depending on conversion efficiencies, nitrogen is usually
mineralized (Wood, 1989). This reasoning may, however, be open to criticism if the
organism selects a subset from the available food for ingestion, with a C:N ratio
different from that of the total food.
Soil food web studies have already advanced theory in ecology in which detritus-based
food webs received little attention until recently (Moore and Hunt, 1988;Moore et al.,
1989). For explaining and predicting decomposition, however, several limitations of
current food web research have still to be overcome.
Firstly, pathogens are not explicitly accounted for, only implicitly, viz. in the nominal
death rate parameters, and some groups such as root herbivores and root symbionts
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like mycorrhizas, which are wide-spread in nature, are seldom addressed. The same
holds for gut symbionts.
Secondly, it is unknown what the composition is (e.g. C:N:P:S ratio) of the organic
material actually used by microorganisms i.e. what enters the food web from detritus
or from root-derived material. This is a fundamental problem which may not be
solved until it is possible to quantify the biomass and activity of various physiological
groups of bacteria and fungi. Perhaps genetic marking and recapture techniques are a
first step that may eventually lead to an identification method of such physiological
groups.
Associated with the question of the composition of food actually ingested is the fact
that there is only scant knowledge on the effects of so-called secondary plant products
(phenolics, terpenoids, alkaloids) on the palatability of organic matter for
microorganisms and soil animals. These substances have a function in protection of
the living plant against diseases and herbivores, but they continue to exert effects after
the plant parts have entered the dead organic matter pool. It seems likely that there is
an evolutionary selective advantage in being able to cope with such substances and it
would be interesting to know at what cost in terms of assimilation and production
efficiencies of the decomposer organisms adaption to such substances takes place and,
indeed, how the evolutionary "necessity" to adapt determines the structure of the
decomposer community and the rate of the decomposition process. The same holds,
likewise, for the array of defense substances, such as antibiotics, used by soil microbes
and animals in the chemical warfare that structures below-ground biological
interactions. Thirdly, non-symbiotic mutualistic relationships other
than
consumption/predation, such as comminution, dispersal and priming of substrates are
not accounted for in current food web research.
Depending on the relative abundance of functional groups and the quality of the
substrate mutualistic relationships have often been shown to increase the microbial
activity. This means that a hitherto unknown part of the decomposition, ascribed to
microorganisms, could rightfully be credited to soil animals. Hence, in food web
simulations, the contributions of soil microorganisms to element transfer is
overestimated and that of animals underestimated. Deletion of a functional group in
food web simulation is one way to better estimate the importance of that group for
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dement transfer (De Ruiter et al., 1992). This has led to as much as an order of
magnitude increase in the estimation of nitrogen transfer by some groups, but the
proportional contribution remains low in most (but not all) cases. However, apart
from consumption/predation, mutualistic effects are still not accounted for by this
technique.
Soil food web research has, in practice, been research on the decomposition of litter
or crop residues. The litter layer, however, is only one of several habitats where
decomposition occurs. Decomposition is already initiated above-ground by
microorganisms on senescing leaves. Small pools in tree stems and branches are
ecosystems in themselves where most of the organic matter produced or introduced is
decomposed. Belowground, the rhizosphere, soil aggregates, worm channels and
termite and ant mounds are important habitats where decomposition takes place in
addition to the litter layer. On the axis from litter layer to insect mounds the habitat
is, to an increasing degree, created by the biota itself: microorganisms -• soil
aggregates; roots -»rhizosphere; worms-»channels; insects •* mounds.
The organisms creating those habitats also create microhabitats for other organisms
with which they often have close mutualistic relationships. On this axis current food
web theory is increasingly difficult to apply as long as mutualistic interactions cannot
be adequately accounted for.
Bearing these limitations in mind one may wonder if food web simulations will ever
reliably represent decomposition and mineralization processes. There is some
evidence they will. In our research on integrated and conventional farming systems
(Brussaard et al., 1988; Kooistra et al., 1989), we are encouraged by the close
agreement between the nitrogen mineralization during the growing season as
simulated from food web interactions with that observed from incubation studies of
field soil (De Ruiter et al., 1992). The clue to this finding may be the sampling
strategy by which all (micro)habitats present on the study site were well represented
in space and time. We sampled at five points in time during the growing season at the
scale of individual plants (Brussaard et al., 1990). We used our organism estimates to
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simulate the nitrogen mineralization on a tens of m2 scale over the entire growing
season, i.e. on one level of scale beyond. If the objective would have been to explain
the decomposition or mineralization process on the scale of the individual plant, we
should have sampled the microsites below the plant scale with a frequency accounting
for the speed at which processes occur in the rhizosphere, soil aggregates, worm
channels, etc. In other words, at a certain hierarchical level decomposition and
mineralization are explained from the level below, given the right sampling strategy.If
beginners' luck has been involved in our result, it probably was in the frequency and
timing of sampling.
Food web simulations may be feasible, but are they necessary? This depends on the
scale at which one is interested in the decomposition process. On a scale of regions
and millennia the climate and edaphic properties such as clay and organic matter
content are usually good enough predictors of the decomposition process. The smaller
the scale, the more important vegetation and resource quality are, followed by the
structure of the decomposer community (Lavelle et al., 1992). All factors acting on a
certain scale influence all scales below. Factors at lower levels may, however, also
modify those at higher levels, perhaps resulting in a genuinely cybernetic system on
the earth scale (cf. the Gaia debate). Irrespective of the spatial and temporal scale,
however, knowledge on the working mechanisms and effects of the chemicals that soil
organisms ingest is important, if we want to know which type of human-imposed
stress, and how much of it, can be added without violating the decomposition process
as a whole. Whatever the stress factor is, in many cases the composition of the
organic matter entering the soil is altered by it, e.g. by increased N or Sdeposition or
greenhouse gases. One example may clarify this point. In the case of added
xenobiotics less effect on sum parameters than on individual parameters has often
been observed, probably due to the funtional replacement of sensitive species by less
sensitive species. In the long run, however, this has been shown to lead to ever
simpler soil communities, in which the energetic costs of adaptation by the surviving
species grow increasingly higher up to the point that the limits to the functioning of
the system have been reached (Van Capelleveen, 1987). To prevent this we have to
increase our insight into the ecophysiology, population biology and adaptive
capabilities of the organisms assembled in functional groups, so as to formulate norms
for setting boundaries on man-induced stress.
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This may be one of the main incentives for the EC to foster the application and
further development of decomposition studies. It is my feeling that for the biological
part of this research food web theory is a useful framework and food web modelling a
useful tool. Further development of this area will undoubtedly benefit from and
contribute to ecological theory, which may, indeed, be one of the main incentives to
foster decomposition research for the ESF.
To summarize, the following research priorities can be identified:
1.
Ecological studies and simulation of mutualistic relationships among
decomposer organisms in key (micro)habitats
2.
Identification of the composition of organic materials actually entering the food
web and ingested within the food web at the functional group level
3.
Evolutionary and ecological effects of secondary plant products on decomposer
organisms and the decomposition process
4.
Isolation and quantification of soil microorganisms at the physiological group
level
REFERENCES
Brussaard L., Kooistra M.J., Lebbink G., Van Veen J.A., 1988. The Dutch
Programme on Soil Ecology of Arable Farming Systems. I. Objectives,
approach and some preliminary results. In: Eijsackers H., Quispel A. (Eds):
Ecological implications of contemporary agriculture. Proc 4th Eur Ecol Symp,
Wageningen, 8-12 Sept 1986.Ecol Bull 39:35-40.
Brussaard L., Bouwman L.A., Geurs M., Hassink J., Zwart K.B., 1990. Biomass,
composition and temporal dynamics of soil organisms of a silt loam soil under
conventional and integrated management. Neth J Agric Sei 38:283-302.
De Ruiter P.C., Moore J.C., Zwart K.B., Bouwman LA., Hassink J., Bloem J., De
Vos J.A., Marinissen J.C.Y., Didden W.A.M., Lebbink G., Brussaard L., 1992.
Simulation of nitrogen mineralization in belowground food webs of two winter
wheat field (submitted).
Hunt H.W., Coleman D.C., Ingham E.R., Ingham R.E., Elliott E.T., Moore J.C., Reid
C.P.P., Morley CR., 1987. The detrital food web in a shortgrass prairie. Biol
Fertil Soils 3:57-68.
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Kooistra M.J., Lebbink G., Brussaard L., 1989. The Dutch Programme on Soil
Ecology of Arable Farming Systems. II. Geogenesis, agricultural history, field
size characteristics and present farming systems at the Lovinkhoeve
experimental farm. Agriculture Ecosystems Environment 27:361-387.
Lavelle P., Dangerfield M., Fragoso G, Lopez-Hernandez D., Eschenbrenner V.,
Brussaard L., 1992.Soil fauna and tropical soil fertility. Chapter 6 in: Ingham
J.S.I., Woomer P.,Swift M.J. (Eds): The biological management of tropical soil
fertility. CAB International, Oxon, UK
Moore J.C., Hunt H.W., 1988. Resource compartmentation and the stability of real
ecosystems. Nature 333: 261-263.
Moore J.C., Walter D.E., Hunt H.W., 1988. Arthropod regulation of micro- and
mesobiota in below-ground detrital food webs.Ann Rev Entomol 33:419-439.
Moore J.C., Walter D.E., Hunt H.W., 1989. Habitat compartmentation and environmental correlates of food chain length. Science 243:238-239.
Paul EA, Clark FE, 1989. Soil microbiology and biochemistry. Ac Press, London etc.,
265 pp.
Stout J.D., Bamforth S.S., Lousier J.D., 1982. Protozoa. In: Page J.F. et al. (Eds),
Methods of soil analysis, Part 2, Chemical and microbiological properties.
Agronomy Monograph no.9, 1103-1121,ASA-SSSA, Madison, USA.
Swift M.J., Heal O.W., Anderson J.M., 1979. Decomposition in terrestrial ecosystems.
Blackwell, Oxford etc., 372pp.
Van Capelleveen H.E., 1987. Ecotoxicity of heavy metals for terrestrial isopods.
Thesis, Free University, Amsterdam, 104pp.
Verhoef H.A., Brussaard L., 1990. Decomposition in natural and agro-ecosystem: the
contribution of soil animals. Biogeochemistry 11: 175-211.
Wood M., 1989.Soil biology, Blackie, Glasgow etc.,UK, 154pp.
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